ALGAE

The Korean Society of Phycology (한국조류학회(藻類))
권호 표지
DOI QR코드

DOI QR Code

Incorporating concepts of biodiversity into modern aquaculture: macroalgal species richness enhances bioremediation efficiency in a lumpfish hatchery

  • Knoop, Jessica (Department of Biosciences, Swansea University) ;
  • Barrento, Sara (Department of Biosciences, Swansea University) ;
  • Lewis, Robert (Department of Biosciences, Swansea University) ;
  • Walter, Bettina (Department of Biosciences, Swansea University) ;
  • Griffin, John N. (Department of Biosciences, Swansea University)
  • Received : 2021.09.22
  • Accepted : 2022.05.12
  • Published : 2022.09.15
Download PDF
⟨ Previous Next ⟩

Abstract

Aquaculture is one of the fastest growing food producing sectors; however, intensive farming techniques of finfish have raised environmental concerns, especially through the release of excessive nutrients into surrounding waters. Biodiversity has been widely shown to enhance ecosystem functions and services, but there has been limited testing or application of this key ecological relationship in aquaculture. This study tested the applicability of the biodiversity-function relationship to integrated multi-trophic aquaculture (IMTA), asking whether species richness can enhance the efficiency of macroalgal bioremediation of wastewater from finfish aquaculture. Five macroalgal species (Chondrus crispus, Fucus serratus, Palmaria palmata, Porphyra dioica, and Ulva sp.) were cultivated in mono- and polyculture in water originating from a lumpfish (Cyclopterus lumpus) hatchery. Total seaweed biomass production, specific growth rates (SGR), and the removal of ammonium (NH4+), total oxidised nitrogen (TON), and phosphate (PO43-) from the wastewater were measured. Species richness increased total seaweed biomass production by 11% above the average component monoculture, driven by an increase in up to 5% in SGR of fast-growing macroalgal species in polycultures. Macroalgal species richness further enhanced ammonium uptake by 25%, and TON uptake by nearly 10%. Phosphate uptake was not improved by increased species richness. The increased uptake of NH4+ and TON with increased macroalgal species richness suggests the complementary use of different nitrogen forms (NH4+ vs. TON) in macroalgal polycultures. The results demonstrate enhanced bioremediation efficiency by increased macroalgal species richness and show the potential of integrating biodiversity-function research to improve aquaculture sustainability.

Keywords

Acknowledgement

The study was funded by a Knowledge Economy Skills Scholarship (KESS)-a pan-Wales higher level skills initiative led by Bangor University on behalf of the HE sector in Wales-partially funded by the Welsh Government's European Social Fund (ESF) convergence programme for West Wales and the Valleys and the Pembrokeshire Beachfood Company. We would further like to thank the team of the Centre for Sustainable Aquatic Research at Swansea University for their technical support.

References

  1. Abreu, M. H., Pereira, R., Yarish, C., Buschmann, A. H. & Sousa-Pinto, I. 2011. IMTA with Gracilaria vermiculophylla: productivity and nutrient removal performance of the seaweed in a land-based pilot scale system. Aquaculture 312:77-87. https://doi.org/10.1016/j.aquaculture.2010.12.036
  2. Anderson, D. M., Glibert, P. M. & Burkholder, J. M. 2002. Harmful algal blooms and eutrophication: nutrient sources, compositions, and consequences. Estuaries 25:704-726. https://doi.org/10.1007/BF02804901
  3. Ashkenazi, D. Y., Israel, A. & Abelson, A. 2018. A novel twostage seaweed integrated multi-trophic aquaculture. Rev. Aquac. 11:246-262. https://doi.org/10.1111/raq.12238
  4. Ashton, I. W., Miller, A. E., Bowman, W. D. & Suding, K. N. 2010. Niche complementarity due to plasticity in resource use: plant partitioning of chemical N forms. Ecology 91:3252-3260. https://doi.org/10.1890/09-1849.1
  5. Barry, K. E., Mommer, L., van Ruijven, J., Wirth, C., Wright, A. J., Bai, Y., Connolly, J., De Deyn, G. B., de Kroon, H., Isbell, F., Milcu, A., Roscher, C., Scherer-Lorenzen, M., Schmid, B. & Weigelt, A. 2019. The future of complementarity: disentangling causes from consequences. Trends Ecol. Evol. 34:167-180. https://doi.org/10.1016/j.tree.2018.10.013
  6. Ben-Ari, T., Neori, A., Ben-Ezra, D., Shauli, L., Odintsov, V. & Shpigel, M. 2014. Management of Ulva lactuca as a biofilter of mariculture effluents in IMTA system. Aquaculture 434:493-498. https://doi.org/10.1016/j.aquaculture.2014.08.034
  7. Bergheim, A., Drengstig, A., Ulgenes, Y. & Fivelstad, S. 2009. Production of Atlantic salmon smolts in Europe: current characteristics and future trends. Aquac. Eng. 41:46-52. https://doi.org/10.1016/j.aquaeng.2009.04.004
  8. Boyer, K. E., Kertesz, J. S. & Bruno, J. F. 2009. Biodiversity effects on productivity and stability of marine macroalgal communities: the role of environmental context. Oikos 118:1062-1072. https://doi.org/10.1111/j.1600-0706.2009.17252.x
  9. Bracken, M. E. S. & Stachowicz, J. J. 2006. Seaweed diversity enhances nitrogen uptake via complementary use of nitrate and ammoniun. Ecology 87:2397-2403. https://doi.org/10.1890/0012-9658(2006)87[2397:SDENUV]2.0.CO;2
  10. Bregnballe, J. 2015. A guide to recirculation aquaculture: an introduction to the new envrionmentally friendly and highly productive closed fish farming systems. Food and Agriculture Organization of the United Nations, Rome, 95 pp.
  11. Britto, D. T. & Kronzucker, H. J. 2002. NH4+ toxicity in higher plants: a critical review. J. Plant Physiol. 159:567-584. https://doi.org/10.1078/0176-1617-0774
  12. Bruno, J. F., Boyer, K. E., Duffy, J. E., Lee, S. C. & Kertesz, J. S. 2005. Effects of macroalgal species identity and richness on primary production in benthic marine communities. Ecol. Lett. 8:1165-1174. https://doi.org/10.1111/j.1461-0248.2005.00823.x
  13. Cardinale, B. J. 2011. Biodiversity improves water quality through niche partitioning. Nature 472:86-89. https://doi.org/10.1038/nature09904
  14. Cardinale, B. J., Srivastava, D. S., Duffy, J. E., Wright, J. P., Downing, A. L., Sankaran, M. & Jouseau, C. 2006. Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989-992. https://doi.org/10.1038/nature05202
  15. Carmona, R., Kraemer, G. P. & Yarish, C. 2006. Exploring Northeast American and Asian species of Porphyra for use in an integrated finfish-algal aquaculture system. Aquaculture 252:54-65. https://doi.org/10.1016/j.aquaculture.2005.11.049
  16. Catarino, M. D., Silva, A. M. S. & Cardoso, S. M. 2018. Phycochemical constituents and biological activities of Fucus spp. Mar. Drugs 16:249. https://doi.org/10.3390/md16080249
  17. Chopin, T. 2017. The renewed interest in the cultivation of seaweeds, as the inorganic extractive component of integrated multi-trophic aquaculture (IMTA) systems, and for the ecosystem services they provide. Bull. Aquac. Assoc. Can. 1:13-18.
  18. Chopin, T., Yarish, C., Wilkes, R., Belyea, E., Lu, S. & Mathieson, A. 1999. Developing Porphyra/salmon integrated aquaculture for bioremediation and diversification of the aquaculture industry. J. Appl. Phycol. 11:463-472. https://doi.org/10.1023/A:1008114112852
  19. Collos, Y. & Harrison, P. J. 2014. Acclimation and toxicity of high ammonium concentrations to unicellular algae. Mar. Pollut. Bull. 80:8-23. https://doi.org/10.1016/j.marpolbul.2014.01.006
  20. Copertino, M. D. S., Tormena, T. & Seeliger, U. 2009. Biofiltering efficiency, uptake and assimilation rates of Ulva clathrata (Roth) J. Agardh (Clorophyceae) cultivated in shrimp aquaculture waste water. J. Appl. Phycol. 21:31-45. https://doi.org/10.1007/s10811-008-9357-x
  21. Corey, P., Kim, J. K., Duston, J. & Garbary, D. J. 2014. Growth and nutrient uptake by Palmaria palmata integrated with Atlantic halibut in a land-based aquaculture system. Algae 29:35-45. https://doi.org/10.4490/algae.2014.29.1.035
  22. de Paula Silva, P. H., McBride, S., de Nys, R. & Paul, N. A. 2008. Integrating filamentous 'green tide' algae into tropical pond-based aquaculture. Aquaculture 284:74-80. https://doi.org/10.1016/j.aquaculture.2008.07.035
  23. Edwards, P. 2015. Aquaculture environment interactions: past, present and likely future trends. Aquaculture 447:2-14. https://doi.org/10.1016/j.aquaculture.2015.02.001
  24. Food and Agriculture Organization of the United Nations. 2020a. Fishery and Aquaculture Statistics (Global capture production 1950-2018) (FishStatJ). Food and Agriculture Organization of the United Nations, Rome.
  25. Food and Agriculture Organization of the United Nations. 2020b. The state of world fisheries and aquaculture 2020: sustainability in action. Food and Agriculture Organization of the United Nations, Rome, 244 pp.
  26. Fortes, M. D. & Luning, K. 1980. Growth rates of North Sea macroalgae in relation to temperature, irradiance and photoperiod. Helgol. Meeresunters. 34:15-29. https://doi.org/10.1007/BF01983538
  27. Fox, J. & Weisberg, S. 2019. An R companion to applied regression. 3rd ed. Sage, Thousand Oaks, CA, 802 pp.
  28. Friedlander, M., Gonen, Y., Kashman, Y. & Beer, S. 1996. Gracilaria conferta and its epiphytes: 3. Allelopathic inhibition of the red seaweed by Ulva cf. lactuca. J. Appl. Phycol. 8:21-25. https://doi.org/10.1007/BF02186217
  29. Gachon, C. M. M., Sime-Ngando, T., Strittmatter, M., Chambouvet, A. & Kim, G. H. 2010. Algal diseases: spotlight on a black box. Trends Plant Sci. 15:633-640. https://doi.org/10.1016/j.tplants.2010.08.005
  30. Gamfeldt, L., Lefcheck, J. S., Byrnes, J. E. K., Cardinale, B. J., Duffy, J. E. & Griffin, J. N. 2015. Marine biodiversity and ecosystem functioning: what's known and what's next? Oikos 124:252-265. https://doi.org/10.1111/oik.01549
  31. Goddek, S., Joyce, A., Kotzen, B. & Burnell, G. M. 2019. Aquaponics food production systems: combined aquaculture and hydroponic production technologies for the future. Springer, Cham, 619 pp.
  32. Grasshoff, K., Ehrhardt, M. & Kremling, K. 1983. Methods of seawater analysis. Verlag Chemie, Weinheim, 419 pp.
  33. Griffen, B. D. 2006. Detecting emergent effects of multiple predator species. Oecologia 148:702-709. https://doi.org/10.1007/s00442-006-0414-3
  34. Griffin, J. N., Mendez, V., Johnson, A. F., Jenkins, S. R. & Foggo, A. 2009. Functional diversity predicts overyielding effect of species combination on primary productivity. Oikos 118:37-44. https://doi.org/10.1111/j.1600-0706.2008.16960.x
  35. Hafting, J. T., Craigie, J. S., Stengel, D. B., Loureiro, R. R., Buschmann, A. H., Yarish, C., Edwards, M. D. & Critchley, A. T. 2015. Prospects and challenges for industrial production of seaweed bioactives. J. Phycol. 51:821-837. https://doi.org/10.1111/jpy.12326
  36. Hale, S. S., Cicchetti, G. & Deacutis, C. F. 2016. Eutrophication and hypoxia diminish ecosystem functions of benthic communities in a New England estuary. Front. Mar. Sci. 3:249.
  37. Hanisak, M. D. & Harlin, M. M. 1978. Uptake of inorganic nitrogen by Codium fragile subsp. tomentosoides (Chlorophyta). J. Phycol. 14:450-454. https://doi.org/10.1111/j.1529-8817.1978.tb02467.x
  38. Harrison, P. J. & Hurd, C. L. 2001. Nutrient physiology of seaweeds: application of concepts to aquaculture. Cah. Biol. Mar. 42:71-82.
  39. Hurd, C. L., Harrison, P. J., Bischof, K. & Lobban, C. S. 2014. Seaweed ecology and physiology. 2nd ed. Cambridge University Press, Cambridge, 551 pp.
  40. Knoop, J. 2019. Establishing the knowledge baseline for sustainable Porphyra cultivation in South Wales. Ph.D. dissertation. Swansea University, Swansea, UK.
  41. Kraemer, G. P., Carmona, R., Chopin, T., Neefus, C., Tang, X. & Yarish, C. 2004. Evaluation of the bioremediatory potential of several species of the red alga Porphyra using short-term measurements of nitrogen uptake as a rapid bioassay. J. Appl. Phycol. 16:489-497. https://doi.org/10.1007/s10811-004-5511-2
  42. Lachnit, T., Blumel, M., Imhoff, J. F. & Wahl, M. 2009. Specific epibacterial communities on macroalgae: phylogeny matters more than habitat. Aquat. Biol. 5:181-186. https://doi.org/10.3354/ab00149
  43. Lefcheck, J. S., Byrnes, J. E. K., Isbell, F., Gamfeldt, L., Griffin, J. N., Eisenhauer, N., Hensel, M. J. S., Hector, A., Cardinale, B. J. & Duffy, J. E. 2015. Biodiversity enhances ecosystem multifunctionality across trophic levels and habitats. Nat. Commun. 6:6936. https://doi.org/10.1038/ncomms7936
  44. Li, H., Zhang, Y., Chen, J., Zheng, X., Liu, F. & Jiao, N. 2019. Nitrogen uptake and assimilation preferences of the main green tide alga Ulva prolifera in the Yellow Sea, China. J. Appl. Phycol. 31:625-635. https://doi.org/10.1007/s10811-018-1575-2
  45. Loreau, M. 1998. Separating sampling and other effects in biodiversity experiments. Oikos 82:600-602. https://doi.org/10.2307/3546381
  46. Loreau, M. & Hector, A. 2001. Partitioning selection and complementarity in biodiversity experiments. Nature 412:72-76. https://doi.org/10.1038/35083573
  47. Macchiavello, J. & Bulboa, C. 2014. Nutrient uptake efficiency of Gracilaria chilensis and Ulva lactuca in an IMTA system with the red abalone Haliotis rufescens. Lat. Am. J. Aquat. Res. 42:523-533. https://doi.org/10.3856/vol42-issue3-fulltext-12
  48. Murray, F., Bostock, J. & Fletcher, D. 2014. Review of recirculation aquaculture system technologies and their commercial application. University of Stirling, Stirling, 75 pp.
  49. Naeem, S., Thompson, L. J., Lawler, S. P., Lawton, J. H. & Woodfin, R. M. 1994. Declining biodiversity can alter the performance of ecosystems. Nature 368:734-737. https://doi.org/10.1038/368734a0
  50. Nilsson, J., Engkvist, R. & Persson, L.-E. 2004. Long-term decline and recent recovery of Fucus populations along the rocky shores of southeast Sweden, Baltic Sea Aquat. Ecol. 38:587-598. https://doi.org/10.1007/s10452-004-5665-7
  51. O'Connor, M. I., Gonzalez, A., Byrnes, J. E. K., Cardinale, B. J., Duffy, J. E., Gamfeldt, L., Griffin, J. N., Hooper, D., Hungate, B. A., Paquette, A., Thompson, P. L., Dee, L. E. & Dolan, K. L. 2017. A general biodiversity-function relationship is mediated by trophic level. Oikos 126:18-31. https://doi.org/10.1111/oik.03652
  52. Patoczka, J. & Wilson, D. J. 1984. Kinetics of the desorption of ammonia from water by diffused aeration. Sep. Sci. Technol. 19:77-93. https://doi.org/10.1080/01496398408059939
  53. Pereira, R., Kraemer, G., Yarish, C. & Sousa-Pinto, I. 2008. Nitrogen uptake by gametophytes of Porphyra dioica (Bangiales, Rhodophyta) under controlled-culture conditions. Eur. J. Phycol. 43:107-118. https://doi.org/10.1080/09670260701763393
  54. Pinheiro, J., Bates, D., DebRoy, S. & Sarkar, D. 2019. nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-139. R Core Team. R Foundation for Statistical Computing, Vienna, Austria.
  55. Powell, A., Treasurer, J. W., Pooley, C. L., Keay, A. J., Lloyd, R., Imsland, A. K. & De Leaniz, C. G. 2018. Use of lumpfish for sea-lice control in salmon farming: challenges and opportunities. Rev. Aquac. 10:683-702. https://doi.org/10.1111/raq.12194
  56. Roleda, M. Y. & Hurd, C. L. 2019. Seaweed nutrient physiology: application of concepts to aquaculture and bioremediation. Phycologia 58:552-562. https://doi.org/10.1080/00318884.2019.1622920
  57. Roleda, M. Y., van de Poll, W. H., Hanelt, D. & Wiencke, C. 2004. PAR and UVBR effects on photosynthesis, viability, growth and DNA in different life stages of two coexisting Gigartinales: implications for recruitment and zonation pattern. Mar. Ecol. Prog. Ser. 281:37-50. https://doi.org/10.3354/meps281037
  58. Ross, M. E., Davis, K., McColl, R., Stanley, M. S., Day, J. G. & Semiao, A. J. C. 2018. Nitrogen uptake by the macro-algae Cladophora coelothrix and Cladophora parriaudii: influence on growth, nitrogen preference and biochemical composition. Algal Res. 30:1-10. https://doi.org/10.1016/j.algal.2017.12.005
  59. Runcie, J. W., Ritchie, R. J. & Larkum, A. W. D. 2003. Uptake kinetics and assimilation of inorganic nitrogen by Catenella nipae and Ulva lactuca. Aquat. Bot. 76:155-174. https://doi.org/10.1016/S0304-3770(03)00037-8
  60. Schmedes, P. S. 2020. Investigating hatchery and cultivation methods for improved cultivation of Palmaria palmata. Ph.D. dissertation. Danish Shellfish Centre, National Institute of Aquatic Resources, Nykobing, 150 pp.
  61. Schmid, B., Baruffol, M., Wang, Z. & Niklaus, P. A. 2017. A guide to analyzing biodiversity experiments. J. Plant Ecol. 10:91-110. https://doi.org/10.1093/jpe/rtw107
  62. Selman, M., Greenhalgh, S., Diaz, R. & Sugg, Z. 2008. Eutrophication and hypoxia in coastal areas: a global assessment of the state of knowledge. World Resources Institute, Washington, DC, 6 pp.
  63. Sharp, G. J. 1987. Growth and production in wild and cultured stocks of Chondrus crispus. Hydrobiologia 151- 152:349-354. https://doi.org/10.1007/BF00046151
  64. Shpirt, E. 1981. Role of hydrodynamic factors in ammonia desorption by diffused aeration. Water Res. 15:739-743. https://doi.org/10.1016/0043-1354(81)90167-6
  65. Stabili, L., Acquaviva, M. I., Angile, F., Cavallo, R. A., Cecere, E., Del Coco, L., Fanizzi, F. P., Gerardi, C., Narracci, M. & Petrocelli, A. 2019. Screening of Chaetomorpha linum lipidic extract as a new potential source of bioactive compounds. Mar. Drugs 17:313. https://doi.org/10.3390/md17060313
  66. Stachowicz, J. J., Graham, M., Bracken, M. E. S. & Szoboszlai, A. I. 2008. Diversity enhances cover and stability of seaweed assemblages: the role of heterogeneity and time. Ecology 89:3008-3019. https://doi.org/10.1890/07-1873.1
  67. Tilman, D. & Downing, J. A. 1994. Biodiversity and stability in grasslands. Nature 367:363-365. https://doi.org/10.1038/367363a0
  68. Tilman, D., Lehman, C. L. & Thomson, K. T. 1997. Plant diversity and ecosystem productivity: theoretical considerations. Proc. Natl. Acad. Sci. U. S. A. 94:1857-1861. https://doi.org/10.1073/pnas.94.5.1857
  69. Tremblay-Gratton, A., Boussin, J. -C., Tamigneaux, E., Vandenberg, G. W. & Le Francois, N. R. 2018. Bioremediation efficiency of Palmaria palmata and Ulva lactuca for use in a fully recirculated cold-seawater naturalistic exhibit: effect of high NO3 and PO4 concentrations and temperature on growth and nutrient uptake. J. Appl. Phycol. 30:1295-1304. https://doi.org/10.1007/s10811-017-1333-x
  70. Vahteri, P. & Vuorinen, I. 2016. Continued decline of the bladderwrack, Fucus vesiculosus, in the Archipelago Sea, northern Baltic proper. Boreal Envrion. Res. 27:373-386.
  71. Voss, M., Bange, H. W., Dippner, J. W., Middelburg, J. J., Montoya, J. P. & Ward, B. 2013. The marine nitrogen cycle: recent discoveries, uncertainties and the potential relevance of climate change. Philos. Trans. R. Soc. B Biol. Sci. 368:20130121. https://doi.org/10.1098/rstb.2013.0121
  72. Zhang, Q. -G. & Zhang, D. -Y. 2006. Resource availability and biodiversity effects on the productivity, temporal variability and resistance of experimental algal communities. Oikos 114:385-396. https://doi.org/10.1111/j.2006.0030-1299.14723.x